Skip to main content
SpringerLink
Log in

Self-Incompatibility in Papaver Rhoeas: Progress in Understanding Mechanisms Involved in Regulating Self-Incompatibility in Papaver

  • Chapter
Self-Incompatibility in Flowering Plants

Abstract

Over the last 20 years or so, our knowledge of what is involved in the rejection of ‘self’ pollen in Papaver rhoeas has expanded tremendously. From initial studies of the population genetics of the S-locus polymorphism, and identification of the pistil S-determinant, the focus has moved to elucidating the signals and mechanisms involved in mediating the inhibition of incompatible pollen tube growth. A key finding was the involvement of a Ca2+-dependent signalling network. This led to the discovery of several SI-induced events, including depolymerisation of the actin cytoskeleton and phosphorylation of a soluble inorganic pyrophosphatase, Prp26.1, which are involved in the rapid inhibition of pollen tube growth. Programmed cell death is also triggered; this provides a neat way to destroy self pollen. Recent studies have begun to unravel components involved in this important event, involving activation of several caspase-like activities. Here we review some of the key findings in recent years.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bosch M, Franklin-Tong VE (2007) Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen. Proc Natl Acad Sci USA 104:18327-18332

    Article  CAS  PubMed  Google Scholar 

  • Bredemeijer GMM, Blaas J (1981) S-Specific proteins in styles of self-incompatible Nicotiana alata. Theor Appl Genet 59:185-190

    Article  CAS  Google Scholar 

  • Campbell JM, Lawrence MJ (1981) The population genetics of the self-incompatibility polymor-phism in Papaver rhoeas. I. The number and distribution of S-alleles in families from three localities. Heredity 46:69-79

    Article  Google Scholar 

  • Clarke SR, Staiger CJ, Gibbon BC, Franklin-Tong VE (1998) A potential signaling role for profilin in pollen of Papaver rhoeas. Plant Cell 10:967-979

    Article  CAS  PubMed  Google Scholar 

  • Dangl JL, Morel J-B (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4:671-683

    Article  PubMed  Google Scholar 

  • de Graaf BHJ, Rudd JJ, Wheeler MJ, Perry RM, Bell EM, Osman K, Franklin FCH, Franklin-Tong VE (2006) Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen. Nature 444:490-493

    Article  CAS  PubMed  Google Scholar 

  • de Nettancourt D (1977) Incompatibility in angiosperms. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Dietrich A, Mayer JE, Hahlbrock K (1990) Fungal elicitor triggers rapid, transient, and specific protein-phosphorylation in parsley cell-suspension cultures. J Biol Chem 265:6360-6368

    CAS  PubMed  Google Scholar 

  • Foote HCC, Ride JP, Franklin-Tong VE, Walker EA, Lawrence MJ, Franklin FCH (1994) Cloning and expression of a distinctive class of self- incompatibility (S) gene from Papaver rhoeas L. Proc Natl Acad Sci USA 91:2265-2269

    Article  CAS  PubMed  Google Scholar 

  • Franklin-Tong VE, Lawrence MJ, Franklin FCH (1988) An in vitro bioassay for the stigmatic product of the self-incompatibility gene in Papaver rhoeas L. New Phytol 110:109-118

    Article  Google Scholar 

  • Franklin-Tong VE, Ride JP, Read ND, Trewavas AJ, Franklin FCH (1993) The self-incompatibility response in Papaver rhoeas is mediated by cytosolic-free calcium. Plant J 4:163-177

    Article  CAS  Google Scholar 

  • Franklin-Tong VE, Ride JP, Franklin FCH (1995) Recombinant stigmatic self-incompatibility-(S-) protein elicits a Ca2+ transient in pollen of Papaver rhoeas. Plant J 8:299-307

    Article  CAS  Google Scholar 

  • Franklin-Tong VE, Hackett G, Hepler PK (1997) Ratio-imaging of[Ca2+ ]i in the self-incompatibility response in pollen tubes of Papaver rhoeas. Plant J 12:1375-1386

    Article  CAS  Google Scholar 

  • Franklin-Tong VE, Holdaway-Clarke TL, Straatman KR, Kunkel JG, Hepler PK (2002) Involve-ment of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas. Plant J 29:333-345

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A, Snowman BN, Emons AMC, Franklin-Tong VE (2000) Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. Plant Cell 12:1239-1251

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A, Franklin-Tong VE, Emons AC (2004) The self-incompatibility response in Papaver rhoeas pollen causes early and striking alterations to organelles. Cell Death Differ 11:812-822

    Article  CAS  PubMed  Google Scholar 

  • Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11:2349-2364

    Article  CAS  PubMed  Google Scholar 

  • Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR (2004) A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 164:803-809

    Article  CAS  PubMed  Google Scholar 

  • Greenberg JT, Guo A, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: A pathogen-triggered response activated co-ordinately with multiple defence functions. Cell 77:551-563

    Article  CAS  PubMed  Google Scholar 

  • Hamel L-P, Nicole M-C, Sritubtim S, Morency M-J, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: Comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192-198

    Article  CAS  PubMed  Google Scholar 

  • Hearn MJ, Franklin, FCH, Ride JP (1996) Identification of a membrane glycoprotein in pollen of Papaver rhoeas which binds stigmatic self-incompatibility (S-) proteins. Plant J 9:467-475

    Article  CAS  Google Scholar 

  • Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401-427

    Article  CAS  PubMed  Google Scholar 

  • Hinata K, Nishio T, Kimura J (1982) Comparative studies on S-glycoproteins purified from differ-ent S-genotypes in self-incompatible Brassica species. II. Immunological specificities. Genetics 100:649-657

    CAS  PubMed  Google Scholar 

  • Huang S, Blanchoin L, Chaudhry F, Franklin-Tong VE, Staiger CJ (2004) A gelsolin-like protein from Papaver rhoeas pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. J Biol Chem 279:23364-23375

    Article  CAS  PubMed  Google Scholar 

  • Jonak C, Ökrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415-424

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Borevitz J, Preuss D (2007) Genome-wide expression profiling of the Ara-bidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genet 3:1848-1861

    Article  CAS  PubMed  Google Scholar 

  • Jordan ND, Kakeda K, Conner A, Ride JP, Franklin-Tong VE, Franklin FCH (1999) S-protein mutants indicate a functional role for SBP in the self-incompatibility reaction of Papaver rhoeas. Plant J 20:119-125

    Article  CAS  PubMed  Google Scholar 

  • Jordan ND, Franklin FCH, Franklin-Tong VE (2000) Evidence for DNA fragmentation triggered in the self- incompatibility response in pollen of Papaver rhoeas. Plant J 23:471-479

    Article  CAS  PubMed  Google Scholar 

  • Kakeda K, Jordan ND, Conner A, Ride JP, Franklin-Tong VE, Franklin FCH (1998) Identification of residues in a hydrophilic loop of the Papaver rhoeas S protein that play a crucial role in recognition of incompatible pollen. Plant Cell 10:1723-1731

    Article  CAS  PubMed  Google Scholar 

  • Korichneva I, Hammerling U (1999) F-actin as a functional target for retro-retinoids: A potential role in anhydroretinol-triggered cell death. J Cell Sci 112:2521-2528

    CAS  PubMed  Google Scholar 

  • Kornberg A (1962) On the metabolic significance of phosphorolytic and pyrophosphorolytic reactions. Academic Press, New York, pp 251-264

    Google Scholar 

  • Kurup S, Ride JP, Jordan N, Fletcher G, Franklin-Tong VE, Franklin FCH (1998) Identification and cloning of related self-incompatibility S- genes in Papaver rhoeas and Papaver nudicaule. Sex Plant Reprod 11:192-198

    Article  CAS  Google Scholar 

  • Lam E, del Pozo O (2000) Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol 44:417-428

    Article  CAS  PubMed  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensi-tive response. Nature 411:848-853

    Article  CAS  PubMed  Google Scholar 

  • Lane MD, Lawrence MJ (1993) The population genetics of the self-incompatibility polymorphism in Papaver Rhoeas. VII. The number of S-alleles in the species. Heredity 71:596-602

    Article  Google Scholar 

  • Lawrence MJ (1975) The genetics of self-incompatibility in Papaver rhoeas. Proc R Soc Lond. Ser B 188:275-285

    Article  Google Scholar 

  • Lawrence MJ, O’Donnell S (1981) The population genetics of the. self-incompatibility polymor-phism in. Papaver rhoeas. III. The number and frequency of S-alleles in two further natural populations (R102 and R104). Heredity 47:53-61

    Article  Google Scholar 

  • Lawrence MJ, Lane MD, O’Donnell S, Franklin-Tong VE (1993) The population-genetics of the self-incompatibility polymorphism in Papaver Rhoeas. V. Cross-classification of the S-alleles of samples from 3 natural-populations. Heredity 71:581-590

    Article  Google Scholar 

  • Lee J, Klessig DF, Nurnberger T (2001) A harpin binding site in tobacco plasma membranes medi-ates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13:1079-1093

    Article  CAS  PubMed  Google Scholar 

  • Li S, Samaj J, Franklin-Tong VE (2007) A mitogen-activated protein kinase signals to programmed cell death induced by self-incompatibility in Papaver pollen. Plant Physiol 145:236-245

    Article  CAS  PubMed  Google Scholar 

  • Malho R, Read ND, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7:1173-1184

    Article  CAS  PubMed  Google Scholar 

  • Mau SL, Raff J, Clarke AE (1982) Isolation and partial characterization of components of Prunus-Avium L styles, including an antigenic glycoprotein associated with a self-incompatibility genotype. Planta 156:505-516

    Article  CAS  Google Scholar 

  • Morley SC, Sun GP, Bierer BE (2003) Inhibition of actin polymerization enhances commitment to and execution of apoptosis induced by withdrawl of trophic support. J Cell Biochem 88:1066-1076

    Article  CAS  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 7:339-346

    Article  Google Scholar 

  • Poulter NS, Vatovec S, Franklin-Tong VE (2008) Microtubules are a target for self-incompatibility signaling in Papaver pollen. Plant Physiol 146:1358-1367

    Article  CAS  PubMed  Google Scholar 

  • Prado AM, Porterfield DM, Feijo JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707-2714

    Article  CAS  PubMed  Google Scholar 

  • Ride JP, Davies EM, Franklin FCH, Marshall DF (1999) Analysis of Arabidopsis genome sequence reveals a large new gene family in plants. Plant Mol Biol 39:927-932

    Article  CAS  PubMed  Google Scholar 

  • Riedl SJ, Shi Y (2004) Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5:897-907

    Article  CAS  PubMed  Google Scholar 

  • Rudd JJ, Franklin-Tong VE (1999) Calcium signaling in plants. Cell Mol Life Sci 55:214-232

    Article  CAS  Google Scholar 

  • Rudd JJ, Franklin FCH, Lord JM, FranklinTong VE (1996) Increased phosphorylation of a 26-kDa pollen protein is induced by the self-incompatibility response in Papaver rhoeas. Plant Cell 8:713-724

    Article  CAS  PubMed  Google Scholar 

  • Rudd JJ, Osman K., Franklin, FCH., Franklin-Tong VE (2003) Activation of a putative MAP kinase in pollen is stimulated by the self-incompatibility (SI) response. FEBS Lett 547:223-227

    Article  CAS  PubMed  Google Scholar 

  • Snowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ (2002) Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell 14:2613-2626

    Article  CAS  PubMed  Google Scholar 

  • Staiger CJ (2000) Signalling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257-288

    Article  CAS  PubMed  Google Scholar 

  • Staiger CJ, Blanchoin L (2006) Actin dynamics: Old friends with new stories. Cell Biol 9:554-562

    CAS  Google Scholar 

  • Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467-489

    Article  CAS  PubMed  Google Scholar 

  • Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136:3864-3876

    Article  CAS  PubMed  Google Scholar 

  • Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305-309

    Article  CAS  PubMed  Google Scholar 

  • Thomas SG, Huang S, Li S, Staiger CJ, Franklin-Tong VE (2006) Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol 174:221-229

    Article  CAS  PubMed  Google Scholar 

  • Walker EA, Ride JP, Kurup S, FranklinTong VE, Lawrence MJ, Franklin FCH (1996) Molec-ular analysis of two functional homologues of the S-3 allele of the Papaver rhoeas self-incompatibility gene isolated from different populations. Plant Mol Biol 30:983-994

    Article  CAS  PubMed  Google Scholar 

  • Wasteneys GO (2003) Microtubules show their sensitive nature. Plant Cell Physiol 44:653-654

    Article  CAS  PubMed  Google Scholar 

  • Woltering EJ (2004) Death proteases come alive. Trends Plant Sci 9:469-472

    Article  CAS  PubMed  Google Scholar 

  • Woltering EJ, van der Bent A, Hoeberichts FA (2002) Do plant caspases exist? Plant Physiol 130:1764-1769

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1939) The distribution of self-sterility alleles in populations. Genetics 24:538-552

    CAS  PubMed  Google Scholar 

  • Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520-527

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

    V. E. Franklin-Tong

Authors
  1. V. E. Franklin-Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Franklin-Tong, V.E. (2008). Self-Incompatibility in Papaver Rhoeas: Progress in Understanding Mechanisms Involved in Regulating Self-Incompatibility in Papaver . In: Self-Incompatibility in Flowering Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-68486-2_11

Download citation

Publish with us

Policies and ethics

Search

Navigation